Microbial - Planktonic foodweb dynamics of a eutrophic Area of Concern: Hamilton Harbour
Keywords:
carbon dynamics, phosphorus, heterotrophy, Great LakesAbstract
Hamilton Harbour, located on the western end of Lake Ontario, has a long history of cultural eutrophication as well as industrial contamination. We explored the structure and function of the microbial – planktonic foodweb during the growing seasons (May–October) of 2004 and 2006 in order to consider the flow of autochthonous production from lower to higher trophic levels. Our analyses included microscope based assessments of bacteria, heterotrophic nanoflagellates, ciliates, phytoplankton and zooplankton as well as radioisotope based measurements of primary productivity and bacterial growth. While routine measures of total phosphorus (avg: 25–33 µg l−1) and chlorophyll a (avg: 12–15 µg l−1) were indicative of eutrophy, mean phytoplankton biomass in 2004 (2.0 g m−3) and 2006 (2.2 g m−3) suggested mesotrophic conditions. However, the appearance of algal blooms in the summer of 2006 was an obvious indicator of cultural eutrophication. With respect to the microbial – planktonic foodweb, the organic carbon pool increased from a mean of 757.5 mg C m−3 in 2004 to 1160.3 mg C m−3 in 2006 and this increase was almost evenly split between autotrophs (198.7 mg C m−3) and heterotrophs (204.1 mg C m−3). The increased autotrophic carbon is readily attributable to the observed algal blooms driven by warmer temperatures and higher concentrations of soluble reactive phosphorus. However, the increase in heterotrophic carbon, primarily heterotrophic nanoflagellates, was apparent from the earliest observations in 2006 and remained consistently high throughout the year. We hypothesize that the increased heterotrophic carbon was the consequence of increased allochthonous carbon being shunted through the microbial foodweb; the energy generated was not likely transferred to zooplankton and passed on to higher trophic levels. More research into the dynamics of allochthonous and autochthonous carbon in eutrophic environments is called for.
References
Anderson, T. and Hessen, D.O., 1991. Carbon, nitrogen and phosphorus content of freshwater zooplankton. Limnol. Oceanogr. 36, 807–813.
Attermeyer, K., Tittel, J., Allgaier, M., Frindte, K., Wurzbacher, C., Hilt, S., Kamjunke, N., Grossart, H-P., 2015. Effects of light and autochthonous carbon additions on microbial turnover of allochthonous organic carbon and community composition. Microb. Ecol. 69, 361–371.
Balcer, M.D., Korda, N.L., Dobson, S.I., 1984. Zooplankton of the Great Lakes: a guide to the identification and ecology of the common crustacean species. The University of Wisconsin Press Ltd, Madison, WI.
Bec, A., Desvilettes, C., Véra, A., Lemarchand, C., Fontvielle, D., Bourdier, G., 2003. Nutritional quality of a freshwater heterotrophic flagellate: trophic upgrading of its microalgal diet for Daphnia hyalina.
Bowen, K., Currie, W., 2017. Elevated zooplankton production in a eutrophic Lake Ontario embayment: Hamilton Harbour 2002–2014. Aquat. Ecosyst. Health Mgmt. 20(3), 230–241.
Brett, M.T., Kainz, M.J., Taipale, S.J., Seshan, H., 2009. Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production. PNAS 106(50), 21197–21201.
Burley, M., 2007. Water quality and phytoplankton photosynthesis. In: R. Dermott, JohannssonO., MunawarM., R. Bonnell, BowenK., BurleyM., FitzpatrickM., J. Gerlofsma, NiblockH. (Eds.), Assessment of lower foodweb in Hamilton Harbour, Lake Ontario, 2002–2004 Can. Tech. Rep. Fish. Aquat. Sci. 2729.
Charlton, M.N., Le Sage, R., 1996. Water quality trends in Hamilton Harbour: 1987 to 1995. Water Qual. Res. J. Canada 31(3), 473–484.
Clarke, R., Somerfield, P., Chapman, M., 2006. On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages. J. Exp. Mar. Biol. Ecol. 330, 55–80.
Collins, M., 1978. Algal toxins. Microbiol. Rev. 42(4), 725–746.
Cyr, H., Pace, M., 1992. Grazing by zooplankton and its relationship to community structure. Can. J. Fish. Aquat. Sci. 49, 1455–1465.
Dermott, R., Johannsson, O., Munawar, M., Bonnell, R., Bowen, K., Burley, M., Fitzpatrick, M., Gerlofsma, J., Niblock, H., 2007. Assessment of lower foodweb in Hamilton Harbour, Lake Ontario, 2002–2004. Can. Tech. Rep. Fish. Aquat. Sci. 2729.
Dodds, W.K., Cole, J.J., 2007. Expanding the concept of trophic state in aquatic ecosystems: it's not just the autotrophs. Aquat. Sci. 69, 427–439.
Ducklow, H., Purdie, D., Williams, P. LeB, Davies, J., 1986. Bacterioplankton: a sink for carbon in a coastal marine plankton community. Science 232, 865–866.
Fermani, P., Diovisalvi, N., Torremorell, A., Lagomarsino, L., Zagarese, H., Unrein, F., 2013. The microbial foodweb structure of a hypertrophic warm-temperate shallow lake, as affected by contrasting zooplankton assemblages. Hydrobiol. 714, 115–130.
Fitzpatrick, M.A.J., Munawar, M., Leach, J.H., and Haffner, G.D., 2007. Factors regulating primary production and phytoplankton dynamics in western Lake Erie. Fundam. Appl. Limnol. (Archiv. Hydrobiol.) 169, 137–152.
Franzé, G., Modigh, M., 2013. Experimental evidence for internal predation in microzooplankton communities. Mar. Biol. 160, 3103–3312.
Gerlofsma, J., Bowen, K., Johannsson, O., 2007. Zooplankton in Hamilton Harbour 2002–2004. In: R. Dermott, JohannssonO., MunawarM., BonnellR., BowenK., BurleyM., FitzpatrickM., GerlofsmaJ., NiblockH. (Eds.), Assessment of lower foodweb in Hamilton Harbour, Lake Ontario, 2002–2004. Can. Tech. Rep. Fish. Aquat. Sci. 2729.
Grigorovich, I. A., MacIsaac, H. J., Rivier, I. K., Aladin, N. V., Panov, V. E., 2000. Comparative biology of the predatory cladoceran Cercopagis pengoi from Lake Ontario, Baltic Sea and the Caspian Lake. Arch. Hydrobiol. 149, 23–50.
Haffner, G.D., Harris, G.P., Jarai, M.K., 1980. Physical variability and phytoplankton communities. III. Vertical structure in phytoplankton populations. Archiv. Hydrobiol. 89(3), 363–381.
Hall, J., O'Connor, K., Ranieri, J., 2006. Progress toward delisting a Great Lakes Area of Concern: the role of integrated research and monitoring in the Hamilton Harbour Remedial Action Plan. Env. Mon. Assmt. 113, 227–243.
Harris, G.P., Piccinin, B.B., 1980. Physical variability and phytoplankton communities: IV. Temporal changes in the phytoplankton community of a physically variable lake. Archiv. Hydrobiol. 89(4), 447–473.
Harris, G.P., Piccinin, B.B., Haffner, G.D., Snodgrass, W., Polak, J., 1980a. Physical variability and phytoplankton communities: I. The descriptive limnology of Hamilton Harbour. Archiv. Hydrobiol. 88(3), 303–327.
Harris, G.P., Haffner, G.D., Piccinin, B.B., 1980b. Physical variability and phytoplankton communities: II. Primary productivity by phytoplankton in a physically variable environment. Archiv. Hydrobiol. 88(4), 393–425.
Heath, R.T., Munawar, M., 2004. Bacterial productivity in Lake Superior, 2001: implications for foodweb efficiencies in oligotrophic freshwater ecosystems. Aquat. Ecosyst. Health. Mgmt. 7(4), 465–474.
Hiriart-Baer, V.P., Diep, N., Smith, R.E.H., 2008. Dissolved organic Matter in the Great Lakes: role and nature of allochthonous material. J. Great Lakes Res. 34, 383–394.
Hiriart-Baer, V.P., Milne, J., Charlton, M.N., 2009. Water quality trends in Hamilton Harbour: two decades of change in nutrients and chlorophyll a. J. Great Lakes Res. 35, 293–301.
Holeck, K.T., Watkins, J.M., Mills, E.L., Johannsson, O., Millard, S., Richardson, V., 2008. Spatial and temporal long term assessment of Lake Ontario water clarity, nutrients, chlorophyll a, and zooplankton. Aquat. Ecosyst. Health. Mgmt. 11(4), 377–391.
Hwang, S-J., Heath, R.T., 1997. Bacterial productivity and protistan bacterivory in coastal and offshore communities of Lake Erie. Can. J. Fish. Aquat. Sci. 54, 788–799.
Hwang, S-J., Heath, R.T., 1999. Zooplankton bacterivory at coastal and offshore sites of Lake Erie. J. Plankton Res. 21(4), 699–719.
International Joint Commission, 1989. Revised Great Lakes Water Quality Agreement of 1978 between the United States and Canada, as amended by protocol, signed November 18, 1987.
Jansson, M., Bergström, Blomqvist, P., Drakare, S., 2000. Allochthonous organic carbon and phytoplankton/bacterioplankton production relationships in lakes. Ecology 81(11), 3250–3255.
Johannsson, O.E., Dermott, R., Graham, D.M., Dahl, J.A., Millard, E.S., Myles, D.D., LeBlanc, J., 2000. Benthic and pelagic secondary production in Lake Erie after the invasion of Dreissena spp. with implications for fish production. J. Great Lakes Res. 26(1), 31–54.
Jørgensen, N.O.G., 1992. Incorporation of [3H] leucine and [3H] valine into protein of freshwater bacteria: field applications. Appl. Environ. Microbiol. 58, 3647–3653.
Jürgens, K., Jeppesen, E., 2000. The impact of metazooplankton on the structure of the microbial foodweb in a shallow, hypertrophic lake. J. Plankton Res. 22(6), 1047–1070.
Jürgens, K., Stolpe, G., 1995. Seasonal dynamics of crustacean zooplankton, heteotrophic nanoflagellates and bacteria in a shallow, eutrophic lake. Freshwat. Biol. 33, 27–38.
Kalinowska, K., Ejsmont-Karabin, J., Rzepecki, M., Kostrzewska-Szlakowska, I., Feniova, I., Palash, A., Dzialowski, A., 2015. Impacts of large bodied crustaceans on the microbial loop. Hydrobiol. 744, 115–125.
Kritzberg, E., Cole, J., Pace, M., Granélil, W., 2005. Does autochthonous primary production drive variability in bacterial metabolism and growth efficiency in lakes dominated by terrestrial C inputs? Aquat. Microb. Ecol. 38, 103–111.
Lee, S., Fuhrman, J.A., 1987. Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl. Env. Microbiol. 53, 1298–1303.
Lund, J.W.G., Kipling, C., LeCren, E.D., 1958. The inverted microscope method of estimating algal numbers and the statistical basis of estimation by counting. Hydrobiol. 9, 143–170.
Lynn, D.H., Munawar, M., 1999. Abundance, biomass, and diversity of planktonic ciliates (Ciliophora) in Lake Erie. In: M. Munawar, T. Edsall and I.F. Munawar (Eds.), State of Lake Erie (SOLE) – past, present and future, pp. 155–168. Backhuys Publishers, Leiden, Netherlands.
Matheson, D.H., 1958. A consolidated report on Burlington Bay. Dept. of Municipal Laboratories, City of Hamilton, Hamilton, ON.
Montagnes, D.J.S. and Lynn, D.H., 1993. A quantitative protargol stain (QPS) for ciliates and other protists. In: P.F. Kemp, B.F. Sherr, SherrE.B., E.J. Cole (Eds.), Handbook of methods in aquatic microbial ecology, pp. 229–240. Lewis Publishers, Boca Raton, FL.
Munawar, M., Fitzpatrick, M., 2007. An integrated assessment of microbial and planktonic communities of Hamilton Harbour. In: R. Dermott, JohannssonO., MunawarM., BonnellR., BowenK., BurleyM., FitzpatrickM., GerlofsmaJ., NiblockH. (Eds.), Assessment of lower foodweb in Hamilton Harbour, Lake Ontario, 2002–2004. Can. Tech. Rep. Fish. Aquat. Sci. 2729.
Munawar, M., Fitzpatrick, M., 2011. The application of Vollenweider's eutrophication models for assessing ecosystem health: Hamilton Harbour (Lake Ontario) example. Aquat. Ecosyst. Health Mgmt. 14(2), 204–208.
Munawar, M., Munawar, I.F., 1976. A lakewide study of phytoplankton biomass and its species composition in Lake Erie, April - December, 1970. J. Fish. Res. Board Can. 33, 581–600.
Munawar, M., Munawar, I.F., 1996. Phytoplankton dynamics in the North American Great Lakes Vol. I: Lakes Ontario, Erie and St. Clair. Ecovision World Monograph Series. SPB Academic Publishing, Amsterdam.
Munawar, M. and Weisse, T., 1989. Is the ‘microbial loop’ an early indicator of anthropogenic stress? Hydrobiol. 188/189, 163–174.
Munawar, M., Munawar, I.F., Fitzpatrick, M., Niblock, H., Bowen, K., Lorimer, J., 2008. An intensive assessment of planktonic communities in the Canadian waters of Lake Erie, 1998. In: Munawar, M. and Heath, R.T. (Eds.), Checking the Pulse of Lake Erie, pp. 297–346. Aquatic Ecosystem Health and Management Society, Burlington, ON, Canada.
Munawar, M., Fitzpatrick, M., Munawar, I.F., Niblock, H., 2010. Checking the pulse of Lake Ontario's microbial-planktonic communities: a trophic transfer hypothesis. Aquat. Ecosyst. Heath. Mgmt. 13, 395–412.
Munawar, M., Fitzpatrick, M., Niblock, H., Lorimer, J., 2011. The relative importance of autotrophic and heterotrophic microbial communities in the planktonic foodweb of the Bay of Quinte, Lake Ontario 2000–2007. Aquat. Ecosyst. Health Mgmt. 14(1), 21–32.
Munawar, M., Fitzpatrick, M., Niblock, H., Kling, H., Rozon, R., Lorimer, J., 2017. Phytoplankton ecology of a culturally eutrophic embayment: Hamilton Harbour, Lake Ontario. Aquat. Ecosyst. Health Mgmt. 20(3), 201–213.
National Laboratory for Environmental Testing (NLET), 1997. Manual of Analytical Methods, Major Ions and Nutrients, Volume 1. Environment Canada, Burlington, Ontario.
Pace, M.L., 1993. Heterotrophic microbial processes. In: CarpenterS.R. and J.F. Kitchell (Eds.), The trophic cascade in lakes, pp. 252–277. Cambridge University Press, Cambridge, UK.
Pace, M.L., Cole, J., Carpenter, S., Kitchell, J., Hodgson, J., Van de Bogert, M., Bade, D., Kritzberg, E., Bastviken, D., 2004. Whole-lake carbon-13 additions reveal terrestrial support of aquatic foodwebs. Nature 427, 240–243.
Painter, D.S., Hampson, L., Millard, E.S., 1990. Hamilton Harbour water clarity response to nutrient abatement. Water Poll. Res. J. Can. 25(3), 351–358.
Pauly, D., and Christensen, V., 1995. Primary production required to sustain global fisheries. Nature 374, 255–257.
Porter, K.G., 1972. A method for the in situ study of zooplankton grazing effects on algal species composition and standing crop. Limnol. Oceanogr. 17, 913–918.
Porter, K.G., 1973. Selective grazing and differential digestion of algae by zooplankton. Nature 244, 179–180.
Porter, K. G., 1996. Integrating the microbial loop and the classic food chanin into a planktonic foodweb. In: Polis, G. A. and Winemiller, K. O. (Eds.), Foodwebs: integration of patterns and dynamics, pp. 51–59. Kluwer Academic Publishers, Boston.
Porter, K.G., Feig, Y.S., 1980. The use of DAPI for identification and enumeration of bacteria and blue-green algae. Limnol. Oceanogr. 25, 943–948.
Poulton, D.J., 1987. Trace contaminant status of Hamilton Harbour. J. Great Lakes Res. 13(2), 193–201.
Redfield, A.C., 1958. The biological control of chemical factors in the environment. American Scientist 46(3), 205–221.
Rodgers, G., Vogt, J., Boyd, D., Simer, L., Lang, H., Murphy, T., Painter, D.S., 1992. Remedial Action Plan for Hamilton Harbour : goals, options and recommendations. ISBN 0-7778-0533-2. Canada-Ontario Agreement respecting Great Lakes water quality.
Sanders, R., Wickham, S., 1993. Planktonic protozoa and metazoan: predation, food quality and population control. Mar. Microb. Foodwebs 7(2), 197–223.
Sanders, R., Cooke, S., Fischer, J., Fey, S., Heinze, A., Jeffrey, W., Macaluso, A., Moeller, R., Morris, D., Neale, P., Olson, M., Pakulski, J., Porter, J., Schoener, D., Williamson, C., 2015. Shifts in microbial foodweb structure and productivity after additions of naturally occurring dissolved organic matter: Results from large-scale lacustrine mesocosms. Limnol. Oceanogr. 60, 2130–2144.
Sherr, E., Sherr, B., 2002. Significance of predation by protists in aquatic microbial foodwebs. Antonie van Leeuwenhoek (J. Microbiol.) 81, 293–308.
Sherr, E., Sherr, B., Albright, L., 1987. Bacteria: link or sink? Science 235, 88.
Smith, E., Prairie, Y., 2004. Bacterial metabolism and growth efficiency in lakes: the importance of phosphorus availability. Limnol. Oceanogr. 49(1), 137–147.
Sprules, W.G., Johannsson, O.E., Millard, E.S., Munawar, M., Stewart, D.S., Tyler, J., Dermott, R., Whipple, S.J., Legner, M., Morris, T.J., Ghan, D., Jech, J.M., 1999. Trophic transfer in Lake Erie: A whole foodweb modeling perspective. A White Paper Submitted for the Great Lakes Modeling Summit. 42nd Conference of the International Association of Great Lakes Research. 1999 May 24–28. Cleveland, OH.
Strathmann, R. R., 1967. Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnol. Oceanogr. 12, 411–418.
Strickland, J.D.H., 1960. Measuring the primary production of marine phytoplankton. Bull. Fish. Res. Board Can. 122.
Strickland, J.D.H., Parsons, T.R., 1968. A practical handbook of seawater analysis. Bulletin of the Fisheries Research Board of Canada, Ottawa, ON, Canada.
Tadonléké, R.D., Pinel-Alloul, B., Bourbonnais, N., and Pick, F.R., 2004. Factors affecting the bacteria – heterotrophic nanoflagellate relationship in oligo-mesotrophic lakes. J. Plankton Res. 26(2), 681–695.
Turley, C.M., Newell, R.C., Robins, D.B., 1986. Survival strategies of two small marine ciliates and their role in regulating bacterial community structure under experimental conditions. Mar. Ecol. Prog. Ser. 33, 59–70.
Utermöhl, H., 1958. Zur vervolkommnung der quantitativen phytoplankton-methodik. Mitt. Internat. Verein. Limnol. 9, 1–38.
Véra, A., Desvilettes, C., Bec, A., Bourdier, G., 2001. Fatty acid composition of freshwater heterotrophic flagellates: an experimental study. Aquat. Microb. Ecol. 25, 271–279.
Verity, P. G., Robertson, C. Y., Tronzo, C. R., Andrews, M. G., Nelson, J. R., Sieracki, M. E., 1992. Relationship between cell volume and the carbon and nitrogen content of marine photosynthetic nanoplankton. Limnol. Oceanogr. 37, 1434–1446.
Weisse, T. and Munawar, M., 1989. Evaluation of the microbial loop in the North American Great Lakes. Can. Tech. Rep. Fish. Aquat. Sci. 1709.
Published
Issue
Section
License
Manuscripts must be original. They must not be published or be under consideration for publication elsewhere, in whole or in part. It is required that the lead author of accepted papers complete and sign the MSU Press AEHM Author Publishing Agreement and provide it to the publisher upon acceptance.
